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Interaction between diabetes mellitus and hypertension on risk of hearing loss in highly endogamous population
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Original article
Interaction between diabetes mellitus and hypertension on risk of hearing loss in highly endogamous population Abdulbari Bener, Advisor Professora,b,* , Abdulla O.A.A. Al-Hamaqc , Khalid Abdulhadid, Ahmed H. Salahaldind , Loida Gansand a
Dept. of Biostatistics & Medical Informatics, Cerrahpaşa Faculty of Medicine, Istanbul University, Istanbul, Turkey Dept. of Evidence for Population Health Unit, School of Epidemiology and Health Sciences, University of Manchester, Manchester, UK Qatar Diabetic Associations and Qatar Foundation, Doha, Qatar d Dept. of ENT, Audiology Unit, Rumailah Hospital & Hamad General Hospital, Hamad Medical Corporation, Qatar b c
A R T I C L E I N F O
A B S T R A C T
Article history: Received 19 August 2016 Accepted 3 September 2016 Available online xxx
Aim: The aim of this study was to determine the prevalence of hearing loss and its association with type 2 diabetes mellitus (T2DM) in a highly endogamous population. Design: This is a cross-sectional study. Setting: The present study is carried out in Ear Nose Throat (ENT) and Endocrinology outpatient clinics of the Hamad General and Rumeilah Hospitals, Hamad Medical Corporation. Subjects: All subjects aged between 20 and 59 years who visited the Endocrinology and ENT outpatient clinics of the Hamad Medical Corporation with hearing difficulty were included in this study during the period from January 2013 to July 2014. Method: During the study period, prevalence, hearing, audiological test, family history and medical problems associated with hearing impairment in middle aged patients were recorded. Two audiometers Grason Stadler GSI 61 and Madsen Orbiter 922 were used to evaluate the hearing loss. Result: Majority of the hearing loss observed at the age above 45 years old, (44.8% vs 51.7%, p = 0.05). The prevalence of hearing impairment was higher in Qataris than in non-Qataris (59.7% vs 46.6%, p < 0.001). The consanguineous marriages were observed higher in Hearing loss (32.1%) than in normal hearing (21.8%) (p = 0.028). The mean of diabetes onset duration (7.8 4.12 years), sleeping disorder (5.81 1.29 h), obese subjects (38% vs 27.4%); family history of diabetes (30.6 vs 23.1%) were higher among hearing impairment. The associated risk factors were significantly higher in T2DM with hearing loss, hypoglycemia (32.8% vs 27.4%), retinopathy (313% vs 18.5%), Nephropathy (17.9% vs 9.8%), Neuropathy (17.9% vs 10.2%), macro-vascular disease (11.9% vs 6.2%), diabetic foot ulcer (20.9% vs 12.6%), Tinnitus (68.7% vs 51.3%), and Vertigo (25.4% vs 16.9%) than in normal hearing diabetes. There was a statistically significant differences between hearing impairment and normal hearing among T2DM regarding hearing assessment frequency (p = 0.041). There were statistically significant differences between hearing impairment versus normal hearing for vitamin D [18.91 7.65 ng/mL vs 22.85 9.00 ng/ mL; p < 0.001], calcium [1.80 0.12 ng/mL vs 1.96 0.14 mmol/L; p < 0.001], magnesium [0.80 0.09 mmol/L vs 0.8 0.14 mmol/L; p < 0.001], phosphorous [1.42 0.30 mmol/L vs 1.56 0.26 mmol/L; p < 0.001], ceatinine [1.42 0.30 mmol/L vs 1.56 0.26 mmol/L; p < 0.001], cholesterol [4.92 1.08 mmol/L vs 4.40 1.01 mmol/L; p = 0.035], LDL [1.92 0.88 mmol/L vs 2.09 0.92 mmol/L; p = 0.024], albumin [43.1 6.10 mmol/L vs 39.8 7.93 mmol/L; p = 0.010], systolic blood pressure [135.8 16.6 Hg vs 130.2 12.5 Hg; p = 0.017] and, diastolic blood pressure [85.1 9.2 mm Hg vs 83.0 7.9 mm Hg; p = 0.012]. There were highly statistically significant differences between hearing impairment versus normal for both side right and left ear frequency in Db unit (p < 0.001). The multivariate stepwise logistic regression analysis revealed that head ache (p < 0.001), family history of DM (p < 0.001), sleep disturbance (p < 0.001), high blood pressure (p = 0.006), consanguinity (p = 0.010), nationality (p = 0.014), age in years (p = 0.025), and sheesha smokers (p = 0.045) were considered at higher risk as a predictors of hearing loss among diabetic patients. Conclusion: The current study results confirm previous reports that adults with DM and hypertension
Keywords: Epidemiology Hearing loss Diabetes Blood glucose Hypertension Risk factors
* Corresponding author at: Dept. of Biostatistics & Medical Informatics, Cerrahpaşa Faculty of Medicine, Istanbul University, 34098 Cerrahpasa, Istanbul, Turkey. E-mail addresses: [email protected], [email protected] (A. Bener). http://dx.doi.org/10.1016/j.dsx.2016.09.004 1871-4021/ã 2016 Diabetes India. Published by Elsevier Ltd. All rights reserved.
Please cite this article in press as: A. Bener, et al., Interaction between diabetes mellitus and hypertension on risk of hearing loss in highly endogamous population, Diab Met Syndr: Clin Res Rev (2016), http://dx.doi.org/10.1016/j.dsx.2016.09.004
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associated showed greater hearing impairment in highly endogamous population . . . Diabetic patients with hearing loss were likely to have high blood glucose and other risk factors like hypertension, retinopathy, nephropathy and neuropathy. ã 2016 Diabetes India. Published by Elsevier Ltd. All rights reserved.
1. Introduction
2.2. Laboratory measurements
Type 2 diabetes mellitus (T2DM), one of the main threats to aging population health in the 21 st century, is described as a worldwide epidemic as it affects the health and economy of almost all countries regardless of socioeconomic status or geographic location [1]. It is based on high blood glucose, insulin resistance and relative insulin deficiency. T2DM leads to an increase in the risk of future cardiovascular disease [2–4] and is the primary reason of death in most high-income and developing countries [3– 5]. Lifestyle factors, sleep duration, physical activity, regular exercise and healthy-balanced diet are essential components in prevention of prediabetes [6–8]. Previous studies of Bener et al. determined a high prevalence of DM in the Qatari population [7,8]. Hearing loss and its complications reveal commonly in type 2 diabetes mellitus (T2DM). Although the prevalence of hearing impairment is increasing in middle age population, unfortunately hearing loss did not accepted as an important problem and often attribute it to increasing age [9–11]. A number of studies have attempted to identify the source of hearing loss in those with DM [9–14]. Several studies investigated that T2DM leads to side effects of hyperglycemia which may be retinopathy, neuropathy, nephropathy, vascular diseases. Thus far, a number of studies reported that increasing sugar levels in the blood damage the nerves and vessels of the inner ear in patients with T2DM [15–17], and it causes an impairment in the auditory system [15]. The researchers often give short change to hearing impairments although hearing loss can affect even the simplest tasks of daily life [17]. The relation between hearing loss and different health conditions among middle aged population is documented and reported in detailed [11–17]. The aim of this study was to determine the prevalence of hearing loss and its association with T2DM among middle aged patients in a highly endogamous population.
The patients were considered to have DM if they have a history of DM and are currently taking oral medications for diabetes. The World Health Organization (WHO) [18] and Bener et al. [19] defined DM when fasting venous blood glucose concentration is equal or higher than 7.0 mmol/L and/or for a 2 h post-glucose tolerance test (GTT) venous blood glucose concentration is higher than 11.1 mmol/L. A glucose meter used to measure fasting blood glucose of all patients. Oral glucose tolerance test (OGTT) was carried out only if blood sugar was less than 7 mmol/L. The inclusion criteria comprised of diagnosis of T2DM in conformity with international standards by WHO [2], fasting plasma glucose (FPG) higher than 7.0 mmol/L and/or 2 h postprandial plasma glucose (PPG) or random plasma glucose higher than 11.1 mmol/L (5). Furthermore, having regular anti-diabetic drug treatment for at least 1 year, aged between 20 and 59 years, residence in a city of Qatari for more than 3 years-period, provided written informed approval to participate in the study were accepted as the inclusion criteria.
2. Subjects and methods This is an observational cohort study which was conducted during the period from January 2013 to July 2014 among diabetic patients aged between 20 and 59 years and registered in diabetic clinics of Hamad General Hospital in Qatar. Only Qatari nationals or non-Qatari Arab ethnicity patients residing in Qatar were included in the present study whereas non-Arab nationals with diabetes were excluded. IRB ethical approval was obtained from Hamad Medical Corporation and PHC Centre before data collection.
2.1. Sampling procedure The current sample size was determined by considering prevalence rate of 10%–12% impaired hearing loss among diabetes patients in Qatar [17], assuming 99% confidence interval and 2% bound on the error of estimation. The minimum sample size detected as 700 subjects. Finally, of the 700 registered with diagnosed diabetes and showed indications, only 459 agreed to participate this study in Hamad General Hospital and PHC Centre, thus it gives a response rate of 65.5%.
2.3. Questionnaire In the first part of the questionnaire, socio-demographic and anthropometric characteristics including age, gender, nationality, education level, height, weight, and parental consanguinity, family history of diabetes, type of diabetes, co-morbid hypertension, and diabetic complications were evaluated. In the second part of the questionnaire, information on lifestyle habits like physical activity and smoking habits were also obtained. In the last part of the questionnaire, information about systolic and diastolic blood pressures, serum triglyceride, total cholesterol, high-density lipoprotein (HDL) cholesterol, low density lipoprotein (LDL) cholesterol, Hemoglobin A1c (HbA1c) and fasting glucose levels (FPG) were collected. 68 subjects were used to test content validity, face validity, and reliability of the questionnaire. A high level of validity and a high degree of repeatability (kappa = 0.85) were found using these tests. The required corrections and modifications have been done after considering the minor differences and discrepancies that have been found during the pilot study. 2.4. Physical examination and measurements A trained nurse evaluated physical examination and measurements. A height scale (SECA, Germany) was used to measure height in centimeters and a weight scale (SECA, Germany) was used to measure weight in kilograms. Thus, BMI was calculated as; weight in kilogram divided by the square of height in meters. According to WHO criteria [20], if it is greater than 25 kg/m2, the subjects were assumed as overweight and greater than to 30 kg/m2, the subjects were considered as obese [19]. WHO [20] International Society of Hypertension Writing Group defined standardized criteria of hypertension when Systolic Blood Pressure (SBP) 140 mmHg or Diastolic Blood Pressure (DBP) 90 mmHg or using anti-hypertensive medication. Using a standard zero mercury sphygmomanometer; systolic (SBP) and diastolic (DBP) blood pressure were measured two times from the subject’s left arm while seated with his/her arm at heart level after at least 10–15 min of rest, and then mean was calculated. Smoking
Please cite this article in press as: A. Bener, et al., Interaction between diabetes mellitus and hypertension on risk of hearing loss in highly endogamous population, Diab Met Syndr: Clin Res Rev (2016), http://dx.doi.org/10.1016/j.dsx.2016.09.004
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habits were classified in terms of currently being smoker or nonsmoker. Patients who walking or cycling for more than 30 min/day were classified as physically active. 2.5. Hearing evaluation procedures Pure-tone audiometry is a behavioral test used to measure hearing sensitivity. This measure involves the peripheral and central auditory systems [21,22]. Pure-tone thresholds (PTTs) indicate the softest sound audible to an individual at least 50% of the time. Hearing sensitivity is plotted on an audiogram, which is a graph displaying intensity as a function of frequency. Two clinical digital audiometers (Garson Stadler GSI 61 and Madsen Orbitar 922 that are regularly calibrated to international standards) were used by pre-trained technicians to test patients’ hearing level in a quiet room. Hearing impairment was defined as the inability to hear a tone of 40 dB or grater at 2000 Hz frequency in the better ear [23]. 2000 Hz is the most important frequency for speech discrimination in the auditory frequency range, therefore it was chosen as the conservative cut point. Hearing loss evaluation described as follows [21–23]: normal (25 dB), mild (26–40 dB), moderate
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(41–55 dB), severe (56–70 dB), very severe (71–90 dB), profound (91–120 dB) and deaf (no hearing). The student t-test was used for assessing the significance of differences between means of two continuous variables and confirmed by non-parametric Mann-Whitney test. Chi-square and Fisher exact tests were performed to test for differences in proportions of categorical variables between two or more groups. Pearson’s correlation coefficient was used to evaluate the strength of concordance between variables. The cut-off value for significance was chosen as 0.05.
3. Results Table 1 shows the socio-demographic characteristics of the studied subjects with hearing loss and normal hearing among T2DM. Majority of the hearing loss observed at the age above 45 years old, (44.8% vs 51.7%, p = 0.05). The prevalence of hearing impairment was higher in Qataris than in non-Qataris (59.7% vs 46.6%, p < 0.001). Over 90% of the studied patients were using mobile phones frequently and 13.4% had hearing impairment
Table 1 Socio demographic characteristics of the subjects and the Prevalence of hearing impairment among diabetics patients (N = 459). Hearing Loss <26 Db n = 134
Normal Hearing >26 Db n = 325
Age Group in years <35 Years 35–44.9 45–55 55 and older
13 (9.7) 25 (18.7) 60(44.8) 36 (26.9)
31 (9.5) 74 (22.8) 118 (51.7) 52 (16)
Gender Male Female
55 (41) 79 (59)
146 (44.9) 179 (55.1)
0.446
Nationality Qatari Non Qatari
80 (59.7) 54 (40.3)
151 (46.5) 174 (53.5)
<0.001
Educational level Illiterate Primary Secondary Primary Secondary
22 (16.4) 30 (22.4) 20 (14.9) 43 (32.1) 19 (14.2)
59 (18.2) 70 (21.5) 68 (20.9) 100 (30.8) 28 (8.6)
Occupation Housewife Sedentary Manual Businessman
87 (64.9) 32 (23.9) 10 (7.55) 5 (3.7)
191 (58.8) 77 (23.7) 47 (14.5) 10(3.1)
Do you use a mobile phone frequently Yes No
121 (90.2) 13 (9.8)
268 (82.5) 57 (17.5)
0.044
Do you hear TV sounds normally Yes No
112(86.6) 22 (13.4)
292 (89.8) 33 (10.2)
0.045
Income <$2000 $2000–$4999 >$5000
49 (36.6) 48 (35.8) 37 (27.6)
112 (34.5) 127(39.1) 86 (26.5)
Consanguineous marriage Yes No
43 (32.1) 91 (67.9)
71 (21.8) 254 (78.2)
Variables
p-value significance
0.05
0.298
0.216
0.806
0.028
Please cite this article in press as: A. Bener, et al., Interaction between diabetes mellitus and hypertension on risk of hearing loss in highly endogamous population, Diab Met Syndr: Clin Res Rev (2016), http://dx.doi.org/10.1016/j.dsx.2016.09.004
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Table 2 Evaluation of hearing loss and its association with T2DM, hypertension and other risk factors. Variables
Hearing Loss <26 Db n = 134 Mean St. Dev
Normal Hearing >26 Db n = 325 Mean St. Dev
P Value
Age in years (mean SD) Hours of sleep (mean SD) Duration of diabetes
48.2 9.0 5.81 1.29 7.8 4.12 n(%)
47.1 8.3 6.17 1.45 6.42 3.25 n(%)
0.176 <0.001 <0.001
BMI Normal (<25 kg/m2) Overweight (25–30 Kg/m2) Obese (30> kg/m2)
32(23.9) 50(37.3) 52(38.8)
77(23.7) 159(48.9) 89(27.4)
0.033
Cigarette smoking Never Current Past
108(81.2) 20(15.0) 5(3.8)
270(83.3) 37(11.4) 17(5.2)
0.478
Sheesha Smoking Yes No
27(20.1) 107(79.9)
41(12.6) 282(87.4)
0.039
Family History of DM Yes No
41(30.6) 93(69.4)
75(23.1) 250(76.9)
<0.001
Diabetes complications Hypoglycemia Retinopathy Nephropathy Neuropathy macro vascular disease Diabetic foot ulcer
44(32.8) 42 (31.3) 24 (17.9) 25 (18) 16 (11.9) 28(20.9)
89 (27.4) 60(18.5) 32 (9.8) 33 (10.2) 20 (6.2) 41 (12.6)
0.024 0.003 0.016 0.022 0.036 0.024
Associated symptoms Excessive passing of urine Excessive thirst Weight loss Loss of appetite Visual disturbance Fatigue Night cramps Sleep loss
35 (26.1) 23 (17.2) 32 (23.9) 48 (35.8) 49 (36.6) 33 (24.6) 18 (13.4) 29 (21.6)
47 (14.5) 45 (13.8) 82 (25.2) 113 (34.8) 79 (24.3) 28 (8.6) 29 (8.9) 31(9.5)
0.003 0.363 0.761 0.830 0.008 0.001 0.147 <0.001
Tinnitus Yes No
89 (68.7) 45 (33.5)
186 (51.1) 159 (48.9)
<0.001
34 (25.4) 100(74.6)
55(16.9) 270 (83.1)
0.050
37 (27.6) 31 (23.1) 28 (20.9) 22 (16.4) 13 (9.7) 4 (3.0)
119 (36.6) 82 (25.3) 57 (17.5) 33 (10.2) 29 (8.9) 5 (1.5)
Vertigo Yes No Hearing evaluation Mild (26–40 dB) Moderate (41–55 dB) Severe (56–70 dB) Very Severe (71–90 dB) Profound (90–120 dB) Deaf (No hearing)
watching TV. The consanguineous marriages were observed higher in Hearing loss (32.1%) than in normal hearing (21.8%) (p = 0.028) Table 2 presents the evaluation of the hearing loss and normal hearing among T2DM and its association with other risk factors. The mean of diabetes onset duration (7.8 4.12 years), sleeping disorder (5.81 1.29 h), obese subjects (38% vs 27.4%); family history of diabetes (30.6 vs 23.1%%) were higher among hearing impairment. The associated risk factors were significantly higher in T2DM with hearing loss, hypoglycemia (32.8% vs 27.4%), retinopathy (313% vs 18.5%), Nephropathy (17.9% vs 9.8%), Neuropathy (17.9% vs 10.2%), macro-vascular disease (11.9% vs 6.2%), diabetic
0.036
foot ulcer (20.9% vs 12.6%), Tinnitus (68.7% vs 51.3%), and Vertigo (25.4% vs 16.9%) than in normal hearing diabetes. There was a statistically significant differences between hearing impairment and normal hearing among T2DM regarding hearing assessment frequency (p = 0.041). Table 3 shows baseline chemistry biomarker values among the two groups. There were statistically significant differences between hearing impairment versus normal hearing for vitamin D [18.91 7.65 ng/mL vs 22.85 9.00 ng/mL; p < 0.001], calcium [1.80 0.12 ng/mL vs 1.96 0.14 mmol/L; p < 0.001], magnesium [0.80 0.09 mmol/L vs 0.8 0.14 mmol/L; p < 0.001], phosphorous
Please cite this article in press as: A. Bener, et al., Interaction between diabetes mellitus and hypertension on risk of hearing loss in highly endogamous population, Diab Met Syndr: Clin Res Rev (2016), http://dx.doi.org/10.1016/j.dsx.2016.09.004
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Table 3 Clinical biochemistry baseline value among Hearing Loss and normal hearing subject. Variables
Hearing Loss <26 Db n = 134 Mean SD
Normal Hearing >26 Db N = 325 Mean SD
P value
Vitamin D (ng/mL) Hemoglobin (g/dL) Magnesium (mmol/L) Potassium (mmol/L) Calcium (mmol/L) Phosphorous (mmol/L) Creatinine(mmol/L) Fasting Blood Glucose(mmol/L) HbA1c Cholesterol (mmol/L) HDL (mmol/L) LDL (mmol/L) Albumin (mmol/L) Billirubin (mmol/L) Triglyceride (mmol/L) Uric Acid (mmol/L) Systolic Blood Pressure mm Hg Diastolic Blood Pressure mm Hg
18.91 7.65 12.75 2.25 0.80 0.09 4.45 0.52 1.80 0.12 1.42 0.30
22.85 9.00 12.90 2.02 0.87 0.08 4.48 0.57 1.96 0.14 1.56 0.26
<0.001 0.296 <0.001 0.215 <0.001 <0.001
9.13 1.68 8.15 1.68 4.92 1.08 1.36 0.45 1.92 0.88 43.1 6.10 8.44 4.21 2.25 0.96 320 112 135.8 16.6 85.1 9.2 n(%) 43(32.0)
8.85 1.80 7.96 1.80 4.40 1.01 1.27 0.37 2.09 0.92 39.8 7.93 7.99 4.54 2.09 0.88 338 108 130.2 12.51 83.0 7.9 n(%) 135(41.5)
0.072 0.188 0.035 0.599 0.024 0.010 0.404 0.549 0.530 0.017 0.012
32(23.8) 29(21.6)
85(26.1) 94(28.9)
<0.001 <0.001
74(55.2)
142(43.7)
45(33.6)
123(37.8)
15(11.2)
60(18.5)
Exposure to sun Walking time per/day <30 min <60 min Vitamin D Level Deficiency 25(OH)D <20 ng/mL Insufficiency 25(OH)D 20–29 ng/mL Optimal 25(OH)D 30–80 ng/mL
[1.42 0.30 mmol/L [1.42 0.30 mmol/L [4.92 1.08 mmol/L [1.92 0.88 mmol/L [43.1 6.10 mmol/L
vs 1.56 0.26 mmol/L; p < 0.001], ceatinine vs 1.56 0.26 mmol/L; p < 0.001], cholesterol vs 4.40 1.01 mmol/L; p = 0.035], LDL vs 2.09 0.92 mmol/L; p = 0.024], albumin vs 39.8 7.93 mmol/L; p = 0.010], systolic
<0.008
<0.045
blood pressure [135.8 16.6 Hg vs 130.2 12.5 Hg; p = 0.017] and, diastolic blood pressure [85.1 9.2 mm Hg vs 83.0 7.9 mm Hg; p = 0.012]. Table 4 presents the mean distribution of Pure Tone Thresholds for both Hearing Loss and normal hearing among Diabetes
Table 4 Mean Pure Tone Thresholds for Hearing Loss and normal hearing among Diabetes subjects. Hearing Loss <26 Db n = 134 Mean SD
Normal Hearing >26 Db N = 325 Mean SD
p-value significance
Side Right Ear (Db) Left Ear (Db)
40.50 17.51 40.90 12.80
18.82 8.10 19.5 8 4.42
<0.001 <0.001
Frequency Side 250 Hz Ri 250 Hz Le 500 Hz Ri 500 Hz Le 1000 Hz Ri 1000 Hz Ri 1500 Hz Ri 1500 Hz Le 2000 Hz Ri 2000 Hz Ri 3000 Hz Ri 3000 Hz Le 4000 Hz Ri 4000 Hz Le 6000 Hz Ri 6000 Hz Le 8000 Hz Ri 8000 Hz Le
43.58 20.80 39.38 14.86 36.83 16.12 34.78 15.83 33.88 21.57 32.28 16.10 28.91 7.65 30.13 1.68 31.90 20.80 33.98 19.77 37.74 21.24 40.23 18.00 43.58 20.91 46.49 16.23 48.41 20.25 52.50 18.07 53.25 19.59 60.52 19.92
22.28 9.14 20.12 5.38 16.85 10.65 14.29 7.02 13.06 9.08 13.15 4.92 12.85 5.10 13.85 4.80 11.09 9.95 13.17 6.25 17.81 8.23 18.85 8.30 21.31 16.24 22.45 12.21 24.83 15.27 29.18 15.79 28.35 16.80 35.92 21.37
<0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001
Variables
Please cite this article in press as: A. Bener, et al., Interaction between diabetes mellitus and hypertension on risk of hearing loss in highly endogamous population, Diab Met Syndr: Clin Res Rev (2016), http://dx.doi.org/10.1016/j.dsx.2016.09.004
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Table 5 Multivariate stepwise logistic regression analysis of variables for predictors of hearing loss among diabetic patients. Variables
Odds Ratio (95%CI)
P value
Head ache Family history of DM Sleep disturbance High Blood pressure Consanguinity Nationality (Qatari) Age in years Sheesha Smoking
2.78(1.63–4.41) 2.56(1.55–4.78) 1.96(1.30–2.82) 1.83(1.20–2.95) 1.68(1.36–2.09) 1.55(1.10–2.17) 1.22(1.10–2.30) 1.60(1.01–2.43)
<0.001 <0.001 <0.001 0.006 0.010 0.014 0.025 0.045
subjects. As can be seen from this table there were highly statistically significant differences between hearing impairment versus normal for both side right and left ear frequency in Db unit (p < 0.001). Table 5 presents multivariate logistic regression analysis of variables for predictors of hearing loss among diabetic patients. Head ache (OR 2.68 95%CI 1.63–4.41; p < 0.001), sleeping disturbance (OR 1.96; 95%CI 1.30–2.82, p < 0.001), family history of DM (OR 2.56 95%CI 1.55–4.78; p < 0.001), having high blood pressure (OR 1.83 95%CI 1.20–2.95; p = 0.006), consanguinity (OR 1.68 95%CI 1.36–2.09; p = 0.010), age in years (OR 1.22; 95%CI 1.10–2.30; p = 0.025), nationality (Qatari) (OR 1.55 95%CI 1.10–2.17; p = 0.014), and sheesha smokers (OR 1.60; 95%CI 1.01–2.43, p = 0.045) were considered at higher risk as a predictors of hearing loss among diabetic patients. 4. Discussion The present study has revealed hearing loss as an important consequence of diabetes indicating metabolic assessment may be useful for diagnosing patients presenting hearing loss. The study also helped to establish the prevalence of otological disorders in diabetic subjects caused by the dysfunction of middle and inner ear. Diabetes was significantly associated with various otological disorders and hearing loss patterns in the age group above 45 years. Therefore, effective control of diabetes is essential to reduce the incidence of deafness in the middle age group to lead a quality life. The prevalence of hearing impairment in the studied subjects was higher in Qatari’s (59.7%) than females (46.5%). Nearly one fourth of the studied diabetics patients suffered from hearing loss which is similar to the findings in some other studies [9,10]. Although comparisons of prevalence rates are difficult because of different methods of assessment and age grouping, the findings of this study are consistent with rates reported elsewhere [9–14]. More recently, Kang et al. [13] reported that HbA1c level was associated with hearing impairment in the non-diabetic participants of current study and therefore the participants with high HbA1c levels could be closely monitored for hearing impairment. A recent meta-analysis concluded that mild hearing loss is more prevalent in participants with DM, which has greater clinical relevance in individuals who are older or who have had DM over a longer duration [14]. The relationship between hearing loss and hypertension is another additional important risk factors. Although the mechanisms that underlie this relationship are poorly understood, a number of studies have indicated that abnormalities of the stria vascularis may play a key role in hypertension-related hearing loss [24,25]. This is consistent with previous reported studies [13,24,25]. Hypertension often coexists with other cardiovascular risk factors such as dyslipidemia or DM, making it more difficult to determine whether hearing loss is definitely cause by
Hypertension, and to evaluate the associations between these other variables. Most previous studies reported that hypertension was associated with high-frequency hearing impairment, and likewise, in this study, we found a positive association between these variables [13]. Histopathological studies have shown damage to the nerves and vessels of the inner ear of individuals with diabetes [13]. Several population-based studies has evaluated the association between diabetes and hearing loss [9–14] and a number of clinical studies have investigated the possible association of diabetes mellitus and hearing loss [11–18]. Audiometric data obtained in this study revealed that hearing became worse as blood sugar increased in subjects. Also, in our study, a good proportion of the subjects with hearing loss were diabetic (32.4%) and hypertensive (32.6%). There is convincing evidence that diabetes-induced microangiopathy, neuropathy, and mitochondrial damage contribute to damage to the auditory system [26]. In NHANES participants aged 40–69 years, the age-adjusted prevalence of diabetes among participants with low to mid frequency hearing impairment was 21.3% among those with diabetes, compared to 9.4% among those without [27]. The association between diabetes and hearing impairment in human subjects has been demonstrated in many (but not all) population-based studies; however, direct comparison of these studies is complicated due to a lack of consistency in the definition of, methodology in diabetes diagnosis, sample demographics, and adjustment for confounding factors. The association between diabetes and hearing impairment tends to be stronger in studies that included younger samples, perhaps because in older samples, other causes of age-related hearing impairment may mask the contribution of diabetes to hearing impairment. The epidemiologic study of the correlation between diabetes and hearing impairment is relatively new. Since most of the clinical human studies published on this subject are cross-sectional analyses, the temporal such as causal relationship between diabetes and hearing impairment has not been clarified. Welldesigned longitudinal studies are necessary in order to explore whether patients with diabetes are at increased risk of early-onset hearing impairment, and whether the progression of hearing impairment varies based on diabetes status, as well as disease management factors, after taking other known contributors to hearing sensitivity into account. Furthermore, type 2 diabetes disproportionately affects the underserved population, and has been identified as the major risk factor for many microvascular diseases [28]. T2DM also affects the vasculature and neural system of the inner ear, often leading to hearing loss, a major risk factor for falls, depression, and other health problems. Based on the evidence on prevalence of hearing impairment among patients with diabetes presented here, it is prudent for clinicians to incorporate auditory function testing as part of the medical management of type 2 diabetes. Though non-modifiable risk factors such as lifetime noise exposure and genetic factors largely contribute to age-related hearing impairment, diabetes prevention efforts, and the careful management of diabetes once diagnosed, can potentially play a role in reducing the burden of disabling hearing impairment in the population. Other associated risk factors in our middle aged subjects with hearing loss were tinnitus (68.7%), retinopathy (31.3%), nephropathy (17.9%), neuropathy (18%), macro vascular disease (11.9%) and vertigo (25.4%). Those results are consistent with the previous reported studies [9–16]. Noise exposure was a main constructional building and environment factors which were frequently associated with sensorineural hearing loss in our study population. Many adults people accept their hearing loss, believing there is no effective treatment; other attribute it to the aging process or even
Please cite this article in press as: A. Bener, et al., Interaction between diabetes mellitus and hypertension on risk of hearing loss in highly endogamous population, Diab Met Syndr: Clin Res Rev (2016), http://dx.doi.org/10.1016/j.dsx.2016.09.004
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deny its existence. Unfortunately many physicians do not view hearing loss as a significant problem and like the patient, often attribute it to normal aging. Finally, this current study was aiming to: increase awareness of the association between T2DM and hearing loss; promote screening for hearing loss; discuss available resources and assistive devices for those with hearing loss; and encourage nurses to take an active role in advocating for assessment and treatment of hearing loss in T2DM patients. 5. Conclusion The current study results confirm previous reports that adults with DM and hypertension associated showed greater hearing impairment in highly endogamous population. Diabetic patients with hearing loss were likely to have high blood glucose and other risk factors like hypertension, retinopathy, nephropathy and neuropathy. Conflict of interest None to declare. Contributors AB designed and supervised the study and was involved in data collection, statistical analysis the writing of the paper. AOAA, KA and LG were involved in data collection, interpretation of data and writing manuscript. All authors approved the final version. Acknowledgments This work was generously supported and funded by the Qatar Diabetes Association, Qatar Foundation. The authors would like to thank the Hamad Medical Corporation for their support and ethical approval (HMC RP# 10213/10 HMC RP# 11147/13 and 13234/13, IRB# 13-00063). References [1] Wild S, Roglic G, Green A, Sicree R, King H. Global prevalence of diabetes – estimates for the year 2000 and projection for 2030. Diabetes Care 2004;27:1047–53. [2] World Health Organization. Definition, Diagnosis and Classification of Diabetes Mellitus and its Complications, Report of a WHO Consultation, WHOINCDINCS/99.2. Geneva; 1999. [3] International diabetes federation. IDF diabetes atlas. 166 Chaussee de La Hulpe B-1170. sixth edition Brussels, Belgium: IDF; 2014. [4] Alberti KG, Zimmet P. Global burden of disease – where does diabetes mellitus fit in. Nat Rev Endocrinol 2013;9:258–60. [5] Bener A, Al-Laftah F, Al-Hamaq AOAA, Daghash M, Abdullatef WK. A study of diabetes complications in an endogamous population: an emerging public health burden. Diabetes Metab Syndr Clin Res Rev 2014;8(2):108–14.
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[6] Bener A, Kim E, Mutlu F, et al. Burden of diabetes mellitus attributable to demographic levels in Qatar: an emerging public health problem. Diabetes Metab Syndr 2014;8(4):216–20. [7] Bener A, Zirie M, Janahi IM, Al Hamaq AOAA, Musallam M, Wareham NJ. Prevalence of diagnosed and undiagnosed diabetes mellitus and its risk factors in a population – based study of Qatar. Diab Res Clin Prac 2009;84:99–106. [8] Bener A, Abdulmalik M, Al-Kazaz M, Mohammed AG, Sanya R, Buhmaid S, et al. Medical audit of the quality of diabetes care: is primary care more successful than outpatient clinics of the hospital. J Prim Care Commun Health 2012;31:42–50. [9] Kakarlapudi V, Sawyer R, Staecker H. The effect of diabetes on sensorineural hearing loss. Otol Neurotol 2003;24:382–6. [10] Austin DF, Konrad-Martin D, Griest S, McMillan GP, McDermott D, Fausti S. Diabetes-related changes in hearing. Laryngoscope 2009;119(September (9)):1788–96. [11] Wackyam PA, Linthicum FH. Diabetes mellitus and hearing loss: clinical and histopathologic relationships. Am J Otol 1986;7:176–82. [12] Frisina ST, Mapes F, Kim S, Frisina DR, Frisina RD. Characterization of hearing loss in aged type II diabetics. Hear Res 2006;211:103–13. [13] Kang SH, Jung da J, Cho KH, Park JW, Lee KY, Do JY. Association between HbA1c level and hearing impairment in a non-diabetic adult population. Metab Syndr Relat Disord 2016;14(March (2)):129–34. [14] Akinpelu OV, Mujica-Mota M, Daniel SJ. Is type 2 diabetes mellitus associated with alternations in hearing? A systematic review and meta-analysis. Laryngoscope 2014;124:767–76. [15] Konrad-Martin D, Austin DF, Griest S, McMillan GP, McDermott D, Fausti S. Diabetes-related changes in auditory brainstem responses. Laryngoscope 2010;120(January (1)):150–8. [16] Ren J, Zhao P, Chen L, Xu A, Brown SN, Xiao X. Hearing loss in middle-aged subjects with type 2 diabetes mellitus. Arch Med Res 2009;40:18–23. [17] Bener A, Bener A, Salahaldin AH, Darwish SM, Gansan L. Association between hearing loss and type 2 diabetes mellitus in elderly people in rapidly developed society. Biomed Res 2008;19(3):187–93. [18] Alberti KG, Zimmet PZ. Definition, diagnosis and classification of diabetes mellitus and its complications. Part 1: diagnosis and classification of diabetes mellitus provisional report of a WHO consultation. Diabet Med 1998;15 (15):539–53. [19] Bener A, Al-Hamaq AOAA, Kurtuluş ME, Abdullatef WK, Zirie M. The role of vitamin D, obesity and physical exercise in regulation of glycemia in Type 2 Diabetes Mellitus patients. Diab Met Syndr Clin Res Rev 2016, doi:http://dx. doi.org/10.1016/j.dsx.2016.06.007. [20] World Health Organization. International society of hypertension writing group: 2003 world health organization (WHO)/International society of hypertension (ISH) statement on management of hypertension. J Hypertens 2003;21:1983–92. [21] Debonis DA, Donohue CL. Survey of Audiology: Fundamentals for Audiologists and Health Professionals. 2nd ed. Allyn & Bacon; 2007. [22] Katz J. Handbook of Clinical Audiology. Baltimore, Md: Lippincott Williams & Wilkins; 2001. [23] Campbell KC. The Basic Audiologic Assessment. Essential Audiology for Physicians. Singular Publishing Group Inc.; 1998. [24] de Moraes Marchiori LL, de Almeida Rego Filho E, Matsuo T. Hypertension as a factor associated with hearing loss. Braz J Otorhinolaryngol 2006;72:533–40. [25] Agarwal S, Mishra A, Jagade M, Kasbekar V, Nagle SK. Effects of hypertension on hearing. Indian J Otolaryngol Head Neck Surg 2013;65(Suppl. 3):614–8. [26] Helzner EP, Contrera KJ. Type 2 diabetes and hearing impairment. Curr Diab Rep 2016;16(January (1)):3, doi:http://dx.doi.org/10.1007/s11892-015-06960. [27] Bainbridge KE, Hoffman HJ, Cowie CC. Diabetes and hearing impairment in the United States: audiometric evidence from the national health and nutrition examination survey, 1999–2004. Ann Intern Med 2008;149:1–10. [28] Calvin D, Watley SR. Diabetes and hearing loss among underserved populations. Nurs Clin North Am 2015;50(September (3)):449–56.
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Diabetes & Metabolic Syndrome: Clinical Research & Reviews xxx (2016) xxx–xxx
Contents lists available at ScienceDirect
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Original article
Interaction between diabetes mellitus and hypertension on risk of hearing loss in highly endogamous population Abdulbari Bener, Advisor Professora,b,* , Abdulla O.A.A. Al-Hamaqc , Khalid Abdulhadid, Ahmed H. Salahaldind , Loida Gansand a
Dept. of Biostatistics & Medical Informatics, Cerrahpaşa Faculty of Medicine, Istanbul University, Istanbul, Turkey Dept. of Evidence for Population Health Unit, School of Epidemiology and Health Sciences, University of Manchester, Manchester, UK Qatar Diabetic Associations and Qatar Foundation, Doha, Qatar d Dept. of ENT, Audiology Unit, Rumailah Hospital & Hamad General Hospital, Hamad Medical Corporation, Qatar b c
A R T I C L E I N F O
A B S T R A C T
Article history: Received 19 August 2016 Accepted 3 September 2016 Available online xxx
Aim: The aim of this study was to determine the prevalence of hearing loss and its association with type 2 diabetes mellitus (T2DM) in a highly endogamous population. Design: This is a cross-sectional study. Setting: The present study is carried out in Ear Nose Throat (ENT) and Endocrinology outpatient clinics of the Hamad General and Rumeilah Hospitals, Hamad Medical Corporation. Subjects: All subjects aged between 20 and 59 years who visited the Endocrinology and ENT outpatient clinics of the Hamad Medical Corporation with hearing difficulty were included in this study during the period from January 2013 to July 2014. Method: During the study period, prevalence, hearing, audiological test, family history and medical problems associated with hearing impairment in middle aged patients were recorded. Two audiometers Grason Stadler GSI 61 and Madsen Orbiter 922 were used to evaluate the hearing loss. Result: Majority of the hearing loss observed at the age above 45 years old, (44.8% vs 51.7%, p = 0.05). The prevalence of hearing impairment was higher in Qataris than in non-Qataris (59.7% vs 46.6%, p < 0.001). The consanguineous marriages were observed higher in Hearing loss (32.1%) than in normal hearing (21.8%) (p = 0.028). The mean of diabetes onset duration (7.8 4.12 years), sleeping disorder (5.81 1.29 h), obese subjects (38% vs 27.4%); family history of diabetes (30.6 vs 23.1%) were higher among hearing impairment. The associated risk factors were significantly higher in T2DM with hearing loss, hypoglycemia (32.8% vs 27.4%), retinopathy (313% vs 18.5%), Nephropathy (17.9% vs 9.8%), Neuropathy (17.9% vs 10.2%), macro-vascular disease (11.9% vs 6.2%), diabetic foot ulcer (20.9% vs 12.6%), Tinnitus (68.7% vs 51.3%), and Vertigo (25.4% vs 16.9%) than in normal hearing diabetes. There was a statistically significant differences between hearing impairment and normal hearing among T2DM regarding hearing assessment frequency (p = 0.041). There were statistically significant differences between hearing impairment versus normal hearing for vitamin D [18.91 7.65 ng/mL vs 22.85 9.00 ng/ mL; p < 0.001], calcium [1.80 0.12 ng/mL vs 1.96 0.14 mmol/L; p < 0.001], magnesium [0.80 0.09 mmol/L vs 0.8 0.14 mmol/L; p < 0.001], phosphorous [1.42 0.30 mmol/L vs 1.56 0.26 mmol/L; p < 0.001], ceatinine [1.42 0.30 mmol/L vs 1.56 0.26 mmol/L; p < 0.001], cholesterol [4.92 1.08 mmol/L vs 4.40 1.01 mmol/L; p = 0.035], LDL [1.92 0.88 mmol/L vs 2.09 0.92 mmol/L; p = 0.024], albumin [43.1 6.10 mmol/L vs 39.8 7.93 mmol/L; p = 0.010], systolic blood pressure [135.8 16.6 Hg vs 130.2 12.5 Hg; p = 0.017] and, diastolic blood pressure [85.1 9.2 mm Hg vs 83.0 7.9 mm Hg; p = 0.012]. There were highly statistically significant differences between hearing impairment versus normal for both side right and left ear frequency in Db unit (p < 0.001). The multivariate stepwise logistic regression analysis revealed that head ache (p < 0.001), family history of DM (p < 0.001), sleep disturbance (p < 0.001), high blood pressure (p = 0.006), consanguinity (p = 0.010), nationality (p = 0.014), age in years (p = 0.025), and sheesha smokers (p = 0.045) were considered at higher risk as a predictors of hearing loss among diabetic patients. Conclusion: The current study results confirm previous reports that adults with DM and hypertension
Keywords: Epidemiology Hearing loss Diabetes Blood glucose Hypertension Risk factors
* Corresponding author at: Dept. of Biostatistics & Medical Informatics, Cerrahpaşa Faculty of Medicine, Istanbul University, 34098 Cerrahpasa, Istanbul, Turkey. E-mail addresses: [email protected], [email protected] (A. Bener). http://dx.doi.org/10.1016/j.dsx.2016.09.004 1871-4021/ã 2016 Diabetes India. Published by Elsevier Ltd. All rights reserved.
Please cite this article in press as: A. Bener, et al., Interaction between diabetes mellitus and hypertension on risk of hearing loss in highly endogamous population, Diab Met Syndr: Clin Res Rev (2016), http://dx.doi.org/10.1016/j.dsx.2016.09.004
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associated showed greater hearing impairment in highly endogamous population . . . Diabetic patients with hearing loss were likely to have high blood glucose and other risk factors like hypertension, retinopathy, nephropathy and neuropathy. ã 2016 Diabetes India. Published by Elsevier Ltd. All rights reserved.
1. Introduction
2.2. Laboratory measurements
Type 2 diabetes mellitus (T2DM), one of the main threats to aging population health in the 21 st century, is described as a worldwide epidemic as it affects the health and economy of almost all countries regardless of socioeconomic status or geographic location [1]. It is based on high blood glucose, insulin resistance and relative insulin deficiency. T2DM leads to an increase in the risk of future cardiovascular disease [2–4] and is the primary reason of death in most high-income and developing countries [3– 5]. Lifestyle factors, sleep duration, physical activity, regular exercise and healthy-balanced diet are essential components in prevention of prediabetes [6–8]. Previous studies of Bener et al. determined a high prevalence of DM in the Qatari population [7,8]. Hearing loss and its complications reveal commonly in type 2 diabetes mellitus (T2DM). Although the prevalence of hearing impairment is increasing in middle age population, unfortunately hearing loss did not accepted as an important problem and often attribute it to increasing age [9–11]. A number of studies have attempted to identify the source of hearing loss in those with DM [9–14]. Several studies investigated that T2DM leads to side effects of hyperglycemia which may be retinopathy, neuropathy, nephropathy, vascular diseases. Thus far, a number of studies reported that increasing sugar levels in the blood damage the nerves and vessels of the inner ear in patients with T2DM [15–17], and it causes an impairment in the auditory system [15]. The researchers often give short change to hearing impairments although hearing loss can affect even the simplest tasks of daily life [17]. The relation between hearing loss and different health conditions among middle aged population is documented and reported in detailed [11–17]. The aim of this study was to determine the prevalence of hearing loss and its association with T2DM among middle aged patients in a highly endogamous population.
The patients were considered to have DM if they have a history of DM and are currently taking oral medications for diabetes. The World Health Organization (WHO) [18] and Bener et al. [19] defined DM when fasting venous blood glucose concentration is equal or higher than 7.0 mmol/L and/or for a 2 h post-glucose tolerance test (GTT) venous blood glucose concentration is higher than 11.1 mmol/L. A glucose meter used to measure fasting blood glucose of all patients. Oral glucose tolerance test (OGTT) was carried out only if blood sugar was less than 7 mmol/L. The inclusion criteria comprised of diagnosis of T2DM in conformity with international standards by WHO [2], fasting plasma glucose (FPG) higher than 7.0 mmol/L and/or 2 h postprandial plasma glucose (PPG) or random plasma glucose higher than 11.1 mmol/L (5). Furthermore, having regular anti-diabetic drug treatment for at least 1 year, aged between 20 and 59 years, residence in a city of Qatari for more than 3 years-period, provided written informed approval to participate in the study were accepted as the inclusion criteria.
2. Subjects and methods This is an observational cohort study which was conducted during the period from January 2013 to July 2014 among diabetic patients aged between 20 and 59 years and registered in diabetic clinics of Hamad General Hospital in Qatar. Only Qatari nationals or non-Qatari Arab ethnicity patients residing in Qatar were included in the present study whereas non-Arab nationals with diabetes were excluded. IRB ethical approval was obtained from Hamad Medical Corporation and PHC Centre before data collection.
2.1. Sampling procedure The current sample size was determined by considering prevalence rate of 10%–12% impaired hearing loss among diabetes patients in Qatar [17], assuming 99% confidence interval and 2% bound on the error of estimation. The minimum sample size detected as 700 subjects. Finally, of the 700 registered with diagnosed diabetes and showed indications, only 459 agreed to participate this study in Hamad General Hospital and PHC Centre, thus it gives a response rate of 65.5%.
2.3. Questionnaire In the first part of the questionnaire, socio-demographic and anthropometric characteristics including age, gender, nationality, education level, height, weight, and parental consanguinity, family history of diabetes, type of diabetes, co-morbid hypertension, and diabetic complications were evaluated. In the second part of the questionnaire, information on lifestyle habits like physical activity and smoking habits were also obtained. In the last part of the questionnaire, information about systolic and diastolic blood pressures, serum triglyceride, total cholesterol, high-density lipoprotein (HDL) cholesterol, low density lipoprotein (LDL) cholesterol, Hemoglobin A1c (HbA1c) and fasting glucose levels (FPG) were collected. 68 subjects were used to test content validity, face validity, and reliability of the questionnaire. A high level of validity and a high degree of repeatability (kappa = 0.85) were found using these tests. The required corrections and modifications have been done after considering the minor differences and discrepancies that have been found during the pilot study. 2.4. Physical examination and measurements A trained nurse evaluated physical examination and measurements. A height scale (SECA, Germany) was used to measure height in centimeters and a weight scale (SECA, Germany) was used to measure weight in kilograms. Thus, BMI was calculated as; weight in kilogram divided by the square of height in meters. According to WHO criteria [20], if it is greater than 25 kg/m2, the subjects were assumed as overweight and greater than to 30 kg/m2, the subjects were considered as obese [19]. WHO [20] International Society of Hypertension Writing Group defined standardized criteria of hypertension when Systolic Blood Pressure (SBP) 140 mmHg or Diastolic Blood Pressure (DBP) 90 mmHg or using anti-hypertensive medication. Using a standard zero mercury sphygmomanometer; systolic (SBP) and diastolic (DBP) blood pressure were measured two times from the subject’s left arm while seated with his/her arm at heart level after at least 10–15 min of rest, and then mean was calculated. Smoking
Please cite this article in press as: A. Bener, et al., Interaction between diabetes mellitus and hypertension on risk of hearing loss in highly endogamous population, Diab Met Syndr: Clin Res Rev (2016), http://dx.doi.org/10.1016/j.dsx.2016.09.004
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habits were classified in terms of currently being smoker or nonsmoker. Patients who walking or cycling for more than 30 min/day were classified as physically active. 2.5. Hearing evaluation procedures Pure-tone audiometry is a behavioral test used to measure hearing sensitivity. This measure involves the peripheral and central auditory systems [21,22]. Pure-tone thresholds (PTTs) indicate the softest sound audible to an individual at least 50% of the time. Hearing sensitivity is plotted on an audiogram, which is a graph displaying intensity as a function of frequency. Two clinical digital audiometers (Garson Stadler GSI 61 and Madsen Orbitar 922 that are regularly calibrated to international standards) were used by pre-trained technicians to test patients’ hearing level in a quiet room. Hearing impairment was defined as the inability to hear a tone of 40 dB or grater at 2000 Hz frequency in the better ear [23]. 2000 Hz is the most important frequency for speech discrimination in the auditory frequency range, therefore it was chosen as the conservative cut point. Hearing loss evaluation described as follows [21–23]: normal (25 dB), mild (26–40 dB), moderate
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(41–55 dB), severe (56–70 dB), very severe (71–90 dB), profound (91–120 dB) and deaf (no hearing). The student t-test was used for assessing the significance of differences between means of two continuous variables and confirmed by non-parametric Mann-Whitney test. Chi-square and Fisher exact tests were performed to test for differences in proportions of categorical variables between two or more groups. Pearson’s correlation coefficient was used to evaluate the strength of concordance between variables. The cut-off value for significance was chosen as 0.05.
3. Results Table 1 shows the socio-demographic characteristics of the studied subjects with hearing loss and normal hearing among T2DM. Majority of the hearing loss observed at the age above 45 years old, (44.8% vs 51.7%, p = 0.05). The prevalence of hearing impairment was higher in Qataris than in non-Qataris (59.7% vs 46.6%, p < 0.001). Over 90% of the studied patients were using mobile phones frequently and 13.4% had hearing impairment
Table 1 Socio demographic characteristics of the subjects and the Prevalence of hearing impairment among diabetics patients (N = 459). Hearing Loss <26 Db n = 134
Normal Hearing >26 Db n = 325
Age Group in years <35 Years 35–44.9 45–55 55 and older
13 (9.7) 25 (18.7) 60(44.8) 36 (26.9)
31 (9.5) 74 (22.8) 118 (51.7) 52 (16)
Gender Male Female
55 (41) 79 (59)
146 (44.9) 179 (55.1)
0.446
Nationality Qatari Non Qatari
80 (59.7) 54 (40.3)
151 (46.5) 174 (53.5)
<0.001
Educational level Illiterate Primary Secondary Primary Secondary
22 (16.4) 30 (22.4) 20 (14.9) 43 (32.1) 19 (14.2)
59 (18.2) 70 (21.5) 68 (20.9) 100 (30.8) 28 (8.6)
Occupation Housewife Sedentary Manual Businessman
87 (64.9) 32 (23.9) 10 (7.55) 5 (3.7)
191 (58.8) 77 (23.7) 47 (14.5) 10(3.1)
Do you use a mobile phone frequently Yes No
121 (90.2) 13 (9.8)
268 (82.5) 57 (17.5)
0.044
Do you hear TV sounds normally Yes No
112(86.6) 22 (13.4)
292 (89.8) 33 (10.2)
0.045
Income <$2000 $2000–$4999 >$5000
49 (36.6) 48 (35.8) 37 (27.6)
112 (34.5) 127(39.1) 86 (26.5)
Consanguineous marriage Yes No
43 (32.1) 91 (67.9)
71 (21.8) 254 (78.2)
Variables
p-value significance
0.05
0.298
0.216
0.806
0.028
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Table 2 Evaluation of hearing loss and its association with T2DM, hypertension and other risk factors. Variables
Hearing Loss <26 Db n = 134 Mean St. Dev
Normal Hearing >26 Db n = 325 Mean St. Dev
P Value
Age in years (mean SD) Hours of sleep (mean SD) Duration of diabetes
48.2 9.0 5.81 1.29 7.8 4.12 n(%)
47.1 8.3 6.17 1.45 6.42 3.25 n(%)
0.176 <0.001 <0.001
BMI Normal (<25 kg/m2) Overweight (25–30 Kg/m2) Obese (30> kg/m2)
32(23.9) 50(37.3) 52(38.8)
77(23.7) 159(48.9) 89(27.4)
0.033
Cigarette smoking Never Current Past
108(81.2) 20(15.0) 5(3.8)
270(83.3) 37(11.4) 17(5.2)
0.478
Sheesha Smoking Yes No
27(20.1) 107(79.9)
41(12.6) 282(87.4)
0.039
Family History of DM Yes No
41(30.6) 93(69.4)
75(23.1) 250(76.9)
<0.001
Diabetes complications Hypoglycemia Retinopathy Nephropathy Neuropathy macro vascular disease Diabetic foot ulcer
44(32.8) 42 (31.3) 24 (17.9) 25 (18) 16 (11.9) 28(20.9)
89 (27.4) 60(18.5) 32 (9.8) 33 (10.2) 20 (6.2) 41 (12.6)
0.024 0.003 0.016 0.022 0.036 0.024
Associated symptoms Excessive passing of urine Excessive thirst Weight loss Loss of appetite Visual disturbance Fatigue Night cramps Sleep loss
35 (26.1) 23 (17.2) 32 (23.9) 48 (35.8) 49 (36.6) 33 (24.6) 18 (13.4) 29 (21.6)
47 (14.5) 45 (13.8) 82 (25.2) 113 (34.8) 79 (24.3) 28 (8.6) 29 (8.9) 31(9.5)
0.003 0.363 0.761 0.830 0.008 0.001 0.147 <0.001
Tinnitus Yes No
89 (68.7) 45 (33.5)
186 (51.1) 159 (48.9)
<0.001
34 (25.4) 100(74.6)
55(16.9) 270 (83.1)
0.050
37 (27.6) 31 (23.1) 28 (20.9) 22 (16.4) 13 (9.7) 4 (3.0)
119 (36.6) 82 (25.3) 57 (17.5) 33 (10.2) 29 (8.9) 5 (1.5)
Vertigo Yes No Hearing evaluation Mild (26–40 dB) Moderate (41–55 dB) Severe (56–70 dB) Very Severe (71–90 dB) Profound (90–120 dB) Deaf (No hearing)
watching TV. The consanguineous marriages were observed higher in Hearing loss (32.1%) than in normal hearing (21.8%) (p = 0.028) Table 2 presents the evaluation of the hearing loss and normal hearing among T2DM and its association with other risk factors. The mean of diabetes onset duration (7.8 4.12 years), sleeping disorder (5.81 1.29 h), obese subjects (38% vs 27.4%); family history of diabetes (30.6 vs 23.1%%) were higher among hearing impairment. The associated risk factors were significantly higher in T2DM with hearing loss, hypoglycemia (32.8% vs 27.4%), retinopathy (313% vs 18.5%), Nephropathy (17.9% vs 9.8%), Neuropathy (17.9% vs 10.2%), macro-vascular disease (11.9% vs 6.2%), diabetic
0.036
foot ulcer (20.9% vs 12.6%), Tinnitus (68.7% vs 51.3%), and Vertigo (25.4% vs 16.9%) than in normal hearing diabetes. There was a statistically significant differences between hearing impairment and normal hearing among T2DM regarding hearing assessment frequency (p = 0.041). Table 3 shows baseline chemistry biomarker values among the two groups. There were statistically significant differences between hearing impairment versus normal hearing for vitamin D [18.91 7.65 ng/mL vs 22.85 9.00 ng/mL; p < 0.001], calcium [1.80 0.12 ng/mL vs 1.96 0.14 mmol/L; p < 0.001], magnesium [0.80 0.09 mmol/L vs 0.8 0.14 mmol/L; p < 0.001], phosphorous
Please cite this article in press as: A. Bener, et al., Interaction between diabetes mellitus and hypertension on risk of hearing loss in highly endogamous population, Diab Met Syndr: Clin Res Rev (2016), http://dx.doi.org/10.1016/j.dsx.2016.09.004
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Table 3 Clinical biochemistry baseline value among Hearing Loss and normal hearing subject. Variables
Hearing Loss <26 Db n = 134 Mean SD
Normal Hearing >26 Db N = 325 Mean SD
P value
Vitamin D (ng/mL) Hemoglobin (g/dL) Magnesium (mmol/L) Potassium (mmol/L) Calcium (mmol/L) Phosphorous (mmol/L) Creatinine(mmol/L) Fasting Blood Glucose(mmol/L) HbA1c Cholesterol (mmol/L) HDL (mmol/L) LDL (mmol/L) Albumin (mmol/L) Billirubin (mmol/L) Triglyceride (mmol/L) Uric Acid (mmol/L) Systolic Blood Pressure mm Hg Diastolic Blood Pressure mm Hg
18.91 7.65 12.75 2.25 0.80 0.09 4.45 0.52 1.80 0.12 1.42 0.30
22.85 9.00 12.90 2.02 0.87 0.08 4.48 0.57 1.96 0.14 1.56 0.26
<0.001 0.296 <0.001 0.215 <0.001 <0.001
9.13 1.68 8.15 1.68 4.92 1.08 1.36 0.45 1.92 0.88 43.1 6.10 8.44 4.21 2.25 0.96 320 112 135.8 16.6 85.1 9.2 n(%) 43(32.0)
8.85 1.80 7.96 1.80 4.40 1.01 1.27 0.37 2.09 0.92 39.8 7.93 7.99 4.54 2.09 0.88 338 108 130.2 12.51 83.0 7.9 n(%) 135(41.5)
0.072 0.188 0.035 0.599 0.024 0.010 0.404 0.549 0.530 0.017 0.012
32(23.8) 29(21.6)
85(26.1) 94(28.9)
<0.001 <0.001
74(55.2)
142(43.7)
45(33.6)
123(37.8)
15(11.2)
60(18.5)
Exposure to sun Walking time per/day <30 min <60 min Vitamin D Level Deficiency 25(OH)D <20 ng/mL Insufficiency 25(OH)D 20–29 ng/mL Optimal 25(OH)D 30–80 ng/mL
[1.42 0.30 mmol/L [1.42 0.30 mmol/L [4.92 1.08 mmol/L [1.92 0.88 mmol/L [43.1 6.10 mmol/L
vs 1.56 0.26 mmol/L; p < 0.001], ceatinine vs 1.56 0.26 mmol/L; p < 0.001], cholesterol vs 4.40 1.01 mmol/L; p = 0.035], LDL vs 2.09 0.92 mmol/L; p = 0.024], albumin vs 39.8 7.93 mmol/L; p = 0.010], systolic
<0.008
<0.045
blood pressure [135.8 16.6 Hg vs 130.2 12.5 Hg; p = 0.017] and, diastolic blood pressure [85.1 9.2 mm Hg vs 83.0 7.9 mm Hg; p = 0.012]. Table 4 presents the mean distribution of Pure Tone Thresholds for both Hearing Loss and normal hearing among Diabetes
Table 4 Mean Pure Tone Thresholds for Hearing Loss and normal hearing among Diabetes subjects. Hearing Loss <26 Db n = 134 Mean SD
Normal Hearing >26 Db N = 325 Mean SD
p-value significance
Side Right Ear (Db) Left Ear (Db)
40.50 17.51 40.90 12.80
18.82 8.10 19.5 8 4.42
<0.001 <0.001
Frequency Side 250 Hz Ri 250 Hz Le 500 Hz Ri 500 Hz Le 1000 Hz Ri 1000 Hz Ri 1500 Hz Ri 1500 Hz Le 2000 Hz Ri 2000 Hz Ri 3000 Hz Ri 3000 Hz Le 4000 Hz Ri 4000 Hz Le 6000 Hz Ri 6000 Hz Le 8000 Hz Ri 8000 Hz Le
43.58 20.80 39.38 14.86 36.83 16.12 34.78 15.83 33.88 21.57 32.28 16.10 28.91 7.65 30.13 1.68 31.90 20.80 33.98 19.77 37.74 21.24 40.23 18.00 43.58 20.91 46.49 16.23 48.41 20.25 52.50 18.07 53.25 19.59 60.52 19.92
22.28 9.14 20.12 5.38 16.85 10.65 14.29 7.02 13.06 9.08 13.15 4.92 12.85 5.10 13.85 4.80 11.09 9.95 13.17 6.25 17.81 8.23 18.85 8.30 21.31 16.24 22.45 12.21 24.83 15.27 29.18 15.79 28.35 16.80 35.92 21.37
<0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001 <0.001
Variables
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Table 5 Multivariate stepwise logistic regression analysis of variables for predictors of hearing loss among diabetic patients. Variables
Odds Ratio (95%CI)
P value
Head ache Family history of DM Sleep disturbance High Blood pressure Consanguinity Nationality (Qatari) Age in years Sheesha Smoking
2.78(1.63–4.41) 2.56(1.55–4.78) 1.96(1.30–2.82) 1.83(1.20–2.95) 1.68(1.36–2.09) 1.55(1.10–2.17) 1.22(1.10–2.30) 1.60(1.01–2.43)
<0.001 <0.001 <0.001 0.006 0.010 0.014 0.025 0.045
subjects. As can be seen from this table there were highly statistically significant differences between hearing impairment versus normal for both side right and left ear frequency in Db unit (p < 0.001). Table 5 presents multivariate logistic regression analysis of variables for predictors of hearing loss among diabetic patients. Head ache (OR 2.68 95%CI 1.63–4.41; p < 0.001), sleeping disturbance (OR 1.96; 95%CI 1.30–2.82, p < 0.001), family history of DM (OR 2.56 95%CI 1.55–4.78; p < 0.001), having high blood pressure (OR 1.83 95%CI 1.20–2.95; p = 0.006), consanguinity (OR 1.68 95%CI 1.36–2.09; p = 0.010), age in years (OR 1.22; 95%CI 1.10–2.30; p = 0.025), nationality (Qatari) (OR 1.55 95%CI 1.10–2.17; p = 0.014), and sheesha smokers (OR 1.60; 95%CI 1.01–2.43, p = 0.045) were considered at higher risk as a predictors of hearing loss among diabetic patients. 4. Discussion The present study has revealed hearing loss as an important consequence of diabetes indicating metabolic assessment may be useful for diagnosing patients presenting hearing loss. The study also helped to establish the prevalence of otological disorders in diabetic subjects caused by the dysfunction of middle and inner ear. Diabetes was significantly associated with various otological disorders and hearing loss patterns in the age group above 45 years. Therefore, effective control of diabetes is essential to reduce the incidence of deafness in the middle age group to lead a quality life. The prevalence of hearing impairment in the studied subjects was higher in Qatari’s (59.7%) than females (46.5%). Nearly one fourth of the studied diabetics patients suffered from hearing loss which is similar to the findings in some other studies [9,10]. Although comparisons of prevalence rates are difficult because of different methods of assessment and age grouping, the findings of this study are consistent with rates reported elsewhere [9–14]. More recently, Kang et al. [13] reported that HbA1c level was associated with hearing impairment in the non-diabetic participants of current study and therefore the participants with high HbA1c levels could be closely monitored for hearing impairment. A recent meta-analysis concluded that mild hearing loss is more prevalent in participants with DM, which has greater clinical relevance in individuals who are older or who have had DM over a longer duration [14]. The relationship between hearing loss and hypertension is another additional important risk factors. Although the mechanisms that underlie this relationship are poorly understood, a number of studies have indicated that abnormalities of the stria vascularis may play a key role in hypertension-related hearing loss [24,25]. This is consistent with previous reported studies [13,24,25]. Hypertension often coexists with other cardiovascular risk factors such as dyslipidemia or DM, making it more difficult to determine whether hearing loss is definitely cause by
Hypertension, and to evaluate the associations between these other variables. Most previous studies reported that hypertension was associated with high-frequency hearing impairment, and likewise, in this study, we found a positive association between these variables [13]. Histopathological studies have shown damage to the nerves and vessels of the inner ear of individuals with diabetes [13]. Several population-based studies has evaluated the association between diabetes and hearing loss [9–14] and a number of clinical studies have investigated the possible association of diabetes mellitus and hearing loss [11–18]. Audiometric data obtained in this study revealed that hearing became worse as blood sugar increased in subjects. Also, in our study, a good proportion of the subjects with hearing loss were diabetic (32.4%) and hypertensive (32.6%). There is convincing evidence that diabetes-induced microangiopathy, neuropathy, and mitochondrial damage contribute to damage to the auditory system [26]. In NHANES participants aged 40–69 years, the age-adjusted prevalence of diabetes among participants with low to mid frequency hearing impairment was 21.3% among those with diabetes, compared to 9.4% among those without [27]. The association between diabetes and hearing impairment in human subjects has been demonstrated in many (but not all) population-based studies; however, direct comparison of these studies is complicated due to a lack of consistency in the definition of, methodology in diabetes diagnosis, sample demographics, and adjustment for confounding factors. The association between diabetes and hearing impairment tends to be stronger in studies that included younger samples, perhaps because in older samples, other causes of age-related hearing impairment may mask the contribution of diabetes to hearing impairment. The epidemiologic study of the correlation between diabetes and hearing impairment is relatively new. Since most of the clinical human studies published on this subject are cross-sectional analyses, the temporal such as causal relationship between diabetes and hearing impairment has not been clarified. Welldesigned longitudinal studies are necessary in order to explore whether patients with diabetes are at increased risk of early-onset hearing impairment, and whether the progression of hearing impairment varies based on diabetes status, as well as disease management factors, after taking other known contributors to hearing sensitivity into account. Furthermore, type 2 diabetes disproportionately affects the underserved population, and has been identified as the major risk factor for many microvascular diseases [28]. T2DM also affects the vasculature and neural system of the inner ear, often leading to hearing loss, a major risk factor for falls, depression, and other health problems. Based on the evidence on prevalence of hearing impairment among patients with diabetes presented here, it is prudent for clinicians to incorporate auditory function testing as part of the medical management of type 2 diabetes. Though non-modifiable risk factors such as lifetime noise exposure and genetic factors largely contribute to age-related hearing impairment, diabetes prevention efforts, and the careful management of diabetes once diagnosed, can potentially play a role in reducing the burden of disabling hearing impairment in the population. Other associated risk factors in our middle aged subjects with hearing loss were tinnitus (68.7%), retinopathy (31.3%), nephropathy (17.9%), neuropathy (18%), macro vascular disease (11.9%) and vertigo (25.4%). Those results are consistent with the previous reported studies [9–16]. Noise exposure was a main constructional building and environment factors which were frequently associated with sensorineural hearing loss in our study population. Many adults people accept their hearing loss, believing there is no effective treatment; other attribute it to the aging process or even
Please cite this article in press as: A. Bener, et al., Interaction between diabetes mellitus and hypertension on risk of hearing loss in highly endogamous population, Diab Met Syndr: Clin Res Rev (2016), http://dx.doi.org/10.1016/j.dsx.2016.09.004
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deny its existence. Unfortunately many physicians do not view hearing loss as a significant problem and like the patient, often attribute it to normal aging. Finally, this current study was aiming to: increase awareness of the association between T2DM and hearing loss; promote screening for hearing loss; discuss available resources and assistive devices for those with hearing loss; and encourage nurses to take an active role in advocating for assessment and treatment of hearing loss in T2DM patients. 5. Conclusion The current study results confirm previous reports that adults with DM and hypertension associated showed greater hearing impairment in highly endogamous population. Diabetic patients with hearing loss were likely to have high blood glucose and other risk factors like hypertension, retinopathy, nephropathy and neuropathy. Conflict of interest None to declare. Contributors AB designed and supervised the study and was involved in data collection, statistical analysis the writing of the paper. AOAA, KA and LG were involved in data collection, interpretation of data and writing manuscript. All authors approved the final version. Acknowledgments This work was generously supported and funded by the Qatar Diabetes Association, Qatar Foundation. The authors would like to thank the Hamad Medical Corporation for their support and ethical approval (HMC RP# 10213/10 HMC RP# 11147/13 and 13234/13, IRB# 13-00063). References [1] Wild S, Roglic G, Green A, Sicree R, King H. Global prevalence of diabetes – estimates for the year 2000 and projection for 2030. Diabetes Care 2004;27:1047–53. [2] World Health Organization. Definition, Diagnosis and Classification of Diabetes Mellitus and its Complications, Report of a WHO Consultation, WHOINCDINCS/99.2. Geneva; 1999. [3] International diabetes federation. IDF diabetes atlas. 166 Chaussee de La Hulpe B-1170. sixth edition Brussels, Belgium: IDF; 2014. [4] Alberti KG, Zimmet P. Global burden of disease – where does diabetes mellitus fit in. Nat Rev Endocrinol 2013;9:258–60. [5] Bener A, Al-Laftah F, Al-Hamaq AOAA, Daghash M, Abdullatef WK. A study of diabetes complications in an endogamous population: an emerging public health burden. Diabetes Metab Syndr Clin Res Rev 2014;8(2):108–14.
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Please cite this article in press as: A. Bener, et al., Interaction between diabetes mellitus and hypertension on risk of hearing loss in highly endogamous population, Diab Met Syndr: Clin Res Rev (2016), http://dx.doi.org/10.1016/j.dsx.2016.09.004